Neural representation in the auditory midbrain of the envelope of vocalizations based on a peripheral ear model

Thilo Rode,Tanja Hartmann,Verena Scheper,Thomas Lenarz,Minoo Lenarz,Hubert H Lim,Peter Hubka,Andrej Kral

doi:10.3389/fncir.2013.00166

Abstract

The auditory midbrain implant (AMI) consists of a single shank array (20 sites) for stimulation along the tonotopic axis of the central nucleus of the inferior colliculus (ICC) and has been safely implanted in deaf patients who cannot benefit from a cochlear implant (CI). The AMI improves lip-reading abilities and environmental awareness in the implanted patients. However, the AMI cannot achieve the high levels of speech perception possible with the CI. It appears the AMI can transmit sufficient spectral cues but with limited temporal cues required for speech understanding. Currently, the AMI uses a CI-based strategy, which was originally designed to stimulate each frequency region along the cochlea with amplitude-modulated pulse trains matching the envelope of the bandpass-filtered sound components. However, it is unclear if this type of stimulation with only a single site within each frequency lamina of the ICC can elicit sufficient temporal cues for speech perception. At least speech understanding in quiet is still possible with envelope cues as low as 50 Hz. Therefore, we investigated how ICC neurons follow the bandpass-filtered envelope structure of natural stimuli in ketamine-anesthetized guinea pigs. We identified a subset of ICC neurons that could closely follow the envelope structure (up to ß100 Hz) of a diverse set of species-specific calls, which was revealed by using a peripheral ear model to estimate the true bandpass-filtered envelopes observed by the brain. Although previous studies have suggested a complex neural transformation from the auditory nerve to the ICC, our data suggest that the brain maintains a robust temporal code in a subset of ICC neurons matching the envelope structure of natural stimuli. Clinically, these findings suggest that a CI-based strategy may still be effective for the AMI if the appropriate neurons are entrained to the envelope of the acoustic stimulus and can transmit sufficient temporal cues to higher centers.

Highlights

An auditory midbrain implant (AMI) designed for stimulation across the central nucleus of the inferior colliculus (ICC) was implanted in deaf patients who could not sufficiently benefit from a cochlear implant (CI; Lim et al, 2007, 2009)
A large percentage of ICC neurons that followed the TSV stimulus with high correlation values were able to closely follow the envelope structure of the other two calls. Based on these findings and previous studies, we propose that there are parallel pathways through the ICC and up to the auditory cortex in which some ICC neurons exhibit complex and transformed spiking patterns while other neurons still transmit a robust temporal representation matching the envelope of a diverse range of complex stimuli
We discuss the implications of these findings for AMI implementation

Summary

Introduction

An auditory midbrain implant (AMI) designed for stimulation across the central nucleus of the inferior colliculus (ICC) was implanted in deaf patients who could not sufficiently benefit from a cochlear implant (CI; Lim et al, 2007, 2009). These patients have neurofibromatosis type 2, which is a genetic disease that leads to bilateral acoustic neuromas. The question arises as to whether such a CI-based strategy is appropriate for the AMI

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Discussion

Conclusion